Trends in Biochemical Sciences
Ancestral lipid biosynthesis and early membrane evolution
Section snippets
Models of the origin of bacterial and archaeal membranes
Three different hypotheses have been recently proposed to explain the origin of G1P and G3P homochiral membranes in archaea and bacteria (Figure 1). First, Koga et al. [7] have proposed that GP was synthesized chemically in a non-chiral manner on pyrite surfaces [7], which would have been the first acellular metabolists, as proposed by Wächtershäuser [8]. A racemic mixture of G1P and G3P could have accumulated in this way and used in phospholipid synthesis during the early emergence of cellular
Genes for stereospecific synthesis of the phospholipid backbone
As we accumulate more complete genome sequences, particularly for prokaryotic species, it becomes possible to look for more- or less-distant homologues to our favourite gene (or gene family) in an attempt to infer evolutionary schemes explaining the origin of this gene according to its distribution and phylogeny. In this way, updated phylogenetic analyses for the genes encoding G1PDH and G3PDH and their homologues should help to elucidate whether the two genes could be far-distant, hardly
Enzyme recruitment from ancestral dehydrogenases at the origin of membrane stereochemistry
As discussed above, G1PDH and G3PDH, which define the specific stereochemistry of archaeal and bacterial membrane lipids, respectively, belong to two large dehydrogenase superfamilies with universal phylogenetic distribution. None of the subfamilies of the G1PDH-type is universal, although the overall occurrence of the superfamily is. It therefore seems that none of the G1PDH-related subfamilies was present in the cenancestor, but rather the cenancestor possessed an ancestral representative
Did the universal cenancestor possess lipid membranes?
Because of the fundamental differences existing between archaeal and bacterial GP lipids, Martin and Russell [9] have proposed that the universal cenancestor lacked membrane lipids. G1PDH and G3PDH might, or might not, have existed at that time, although, as we have discussed above, related members had already evolved that could have been capable of non-stereospecific GP synthesis. In addition, a few genes encoding enzymes participating in isoprenoid biosynthesis also seem to be ancestral,
Perspectives
The evolutionary genesis of lipid membranes is still a mystery, and lipids are often omitted in early evolutionary models. A few authors have discussed the origin and evolution of lipids and their metabolic synthesis 8, 33, 34 but, in general, their propositions are theoretical bottom-up models. In any case, the presence of amphiphilic components, including long-chain acids and alcohols, in meteorites attests for their abiotic synthesis, which indicates that lipids might have been formed under
Acknowledgements
We acknowledge the constructive criticisms received from two anonymous reviewers. This work was supported by an ATIP grant from the Centre National de la Recherche Scientifique to P.L.G. J.P. enjoyed the hospitality of the Département d'Evolution et Systématique at the Université de Paris-Sud during a sabbatical leave of absence from the Universitat de València and was recipient of a postdoctoral fellowship from Generalitat Valenciana.
Glossary
- Amphipatic:
- Possessing a hydrophobic (water-repelling) and a hydrophilic (water-soluble) region.
- Cenancestor:
- The most recent common ancestor of the taxa under consideration.
- Chiral:
- A molecule is chiral (i.e. it has chirality) if its image in a plane mirror cannot be brought to coincide with itself.
- Enantiomers:
- Synonymous with stereoisomers (see ‘stereochemistry’).
- Enzyme recruitment:
- Development of a new enzymatic activity from a functionally related enzyme derived from gene duplication.
- Heterochiral:
References (40)
Aquifex pyrophilus gen. nov., sp. nov., represents a novel group of marine hyperthermophilic hydrogen-oxiding bacteria
Syst. Appl. Microbiol.
(1992)Phospholipid etherlipid and phospholipid fatty acid fingerprints in selected euryarchaeotal monocultures for taxonomic profiling
FEMS Microbiol. Lett.
(2002)- et al.
Horizontal gene transfer and phylogenetics
Curr. Opin. Microbiol.
(2003) Glycerol dehydrogenase: structure, specificity, and mechanism of a family III polyol dehydrogenase
Structure
(2001)Crystal structure of Pseudomonas fluorescens mannitol 2-dehydrogenase: evidence for a very divergent long-chain dehydrogenase family
Chem. Biol. Interact.
(2003)- et al.
β-Oxidation – strategies for the metabolism of a wide variety of acyl-CoA esters
Biochim. Biophys. Acta
(2000) Towards reconstruction of ancestral genomes by gene cluster alignment
Syst. Appl. Microbiol.
(1998)- et al.
Missing genes in metabolic pathways: a comparative genomics approach
Curr. Opin. Chem. Biol.
(2003) - et al.
The terpenoid theory of the origin of cellular life: the evolution of terpenoids to cholesterol
Chem. Biol.
(1994) - et al.
Archaeal genomics: an overview
Cell
(1997)
Escherichia coli DnaA protein-phospholipid interactions: in vitro and in vivo
Biochimie
The phytanyl ether-linked polar lipids and isoprenoid neutral lipids of extremely halophilic bacteria
Prog. Chem. Fats Other Lipids
Membrane lipids of archaea
Ether Lipids: Biochemical and Biomedical Aspects
Analysis of membrane stereochemistry with homology modeling of sn-glycerol-1-phosphate dehydrogenase
Protein Eng.
Did archaeal and bacterial cells arise independently from noncellular precursors? A hypothesis stating that the advent of membrane phospholipid with enantiomeric glycerophosphate backbones caused the separation of the two lines of descent
J. Mol. Evol.
Before enzymes and templates: theory of surface metabolism
Microbiol. Rev.
On the origins of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells
Philos. Trans. R. Soc. London Ser. B
Pyrite and the origin of life
Nature
The emergence of life from iron monosulfide bubbles at a submarine hydrothermal redox and pH front
J. Geol. Soc. Lond.
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